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The European Eel (Anguilla Anguilla L.) Its 12 Lifecycle and Reproduction; Possible Causes for Decline of Eel Populations

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The European Eel (Anguilla Anguilla L.) Its 12 Lifecycle and Reproduction; Possible Causes for Decline of Eel Populations Simulated Migration of European Eel (Anguilla anguilla, Linnaeus 1758) Promotor Prof.Dr.Johan A.J. Verreth Hoogleraar in de Aquacultuur en Visserij Wageningen Universiteit Co-promotor Dr. Guido E.E.J.M. van den Thillart Universitair Hoofd Docent, Instituut Biologie, Universiteit Leiden Promotiecommissie Prof. Dr. Ir. M. W. A. Verstegen (Wageningen Universiteit) Dr. A. J. Murk (Wageningen Universiteit) Prof. Dr. S. E. Wendelaar Bonga (Radboud Universiteit Nijmegen) Dr. S. Dufour (National Center of Scientific Research, MNHN Paris, France) Simulated Migration of European Eel (Anguilla anguilla, Linnaeus 1758) Vincentius Johannes Theodor van Ginneken Proefschrift Ter verkrijging van de graad van Doctor op gezag van de Rector Magnificus van Wageningen Universiteit Prof.Dr. M.J.Kropff in het openbaar te verdedigen op woensdag 14 juni 2006 des namiddags te half twee in de Aula Van Ginneken, V.J.T. Simulated migration of European eel (Anguilla anguilla, Linnaeus 1758) PhD Thesis, Wageningen University, The Netherlands With ref.- With summary in English, and Dutch ISBN: 90-8504-456-1 Daarom wordt mij verschillende malen te verstaan gegeven, dat ik, waar ik zo stellig het ontstaan door voortteling beweer, de wijze van voortteling van de alen zou moeten aantonen, hoofdzakelijk daarom, omdat het grootste deel van de mensen stellig gelooft, dat de alen zonder het middel der voortteling voortkomen; alsof ik in staat moest zijn, in geval ik zodanige bovengenoemde stellingen volhield, op te lossen al hetgeen omtrent genoemd onderwerp mij werd voorgelegd. Hoewel het veld van de dingen die tot nog toe in het duister verborgen zijn, zo ruim en wijd is. Niettemin heb ik enige jaren reeds alle moeite gedaan om, indien het mogelijk was, de voortteling der Alen te ontdekken en haar voor de ogen van de Wereld te plaatsen. (Antoni van Leeuwenhoek, Brief No. 115, 18 september 1691). Contents Samenvatting 1 Summary 7 Chapter 1. General Introduction: The European eel (Anguilla Anguilla L.) its 12 lifecycle and reproduction; possible causes for decline of eel populations. Chapter 1. Aims and outline of the Thesis 32 Chapter 2. Microelectronic detection of activity level and magnetic orientation of 35 yellow European eel, Anguilla anguilla L., in a pond. Chapter 3. Silvering of European eel (Anguilla anguilla L.): seasonal changes of 50 morphological and metabolic parameters. Chapter4. Endocrine and metabolic profiles during silvering of the European eel 69 (Anguilla anguilla L.). Chapter 5. Direct calorimetry of free moving eels with manipulated thyroid status. 85 Chapter 6. Endurance swimming of European eel 97 Chapter 7. Acute stress syndrome of the yellow European eel 109 (Anguilla anguilla Linnaeus) when exposed to a graded swimming-load Chapter 8. Eel fat stores are enough to reach the Sargasso 125 Chapter 9. Eel migration to the Sargasso: remarkably high swimming efficiency 129 and low energy costs. Chapter 10. Hematology patterns of migrating European eels 146 and the role of EVEX virus Chapter 11. Presence of eel viruses in eel species from various geographic regions 160 Chapter 12. Effects of PCBs on the energy cost of migration and blood parameters of 167 European silver eel (Anguilla anguilla, Linnaeus 1758) Chapter 13. A 5,500-km swim trial stimulates gonad maturation 189 in the European eel (Anguilla anguilla L.) Chapter 14. Recommendations for protection of the eel populations and 212 suggestions for future research Annex 1. The European eel (Anguilla anguilla, Linnaeus), its lifecycle, 229 Evolution and reproduction: a literature review Annex 2. Gonad development and spawning behavior of 279 artificially-matured European eel (Anguilla anguilla L.). Annex 3. Publicity disseminations (news papers, TV, Radio etc.) 299 Annex 4. List of publications 301 Annex 5. Curriculum Vitae 305 Dankwoord 307 Samenvatting Samenvatting proefschrift “Gesimuleerde migratie van de Europese aal (Anguilla anguilla L.)” Introductie Over de laatste 25 jaar is de populatie van de Europese paling is zo'n sterke mate afgenomen dat er grote zorgen zijn ontstaan om zijn voortbestaan op de lange termijn. Populaties van volwassen dieren begonnen af te nemen vanaf 1940 in grote delen van het Europees continent, terwijl het recruitment (aanwas via golven van glasaal) vanaf de jaren tachtig van de vorige eeuw zijn afgenomen. Tot op heden zijn er geen signalen van herstel en dit fenomeen kan gesignaleerd worden over het hele levensgebied van de Europese paling. Een parallelle ontwikkeling kan worden geobserveerd voor de nauw verwante Amerikaanse paling (A.rostrata) en de Japanse paling (A.japonica). De Europese paling (Anguilla anguilla L.) is een katadrome vissoort met zijn paaigebieden duizenden kilometers ver in de oceaan. Een belangrijk aspect van de reproductie van de Europese paling is de enorme afstand die zij moeten zwemmen om hun paaigebieden te bereiken. Na het verlaten van de Europese kusten moeten ze 5000-6000 km zwemmen om de Sargasso Zee te bereiken. Van deze zee wordt aangenomen dat hier de paaigronden liggen. Om deze enorme afstand af te leggen moeten de alen 6 maanden lang bij een 0.5 lichaamslengte per seconde zwemmen wat een indrukwekkende lange termijn zweminspanning vereist. Daarnaast zijn grote energievoorraden gekoppeld met lage energiekosten voor transport vereist. Hieraan kan de hypothese worden toegevoegd dat lange termijn zwemmen een belangrijke voorwaarde kan zijn voor reproductie. In dit proefschrift hebben we de capaciteit van Europese paling onderzocht om over deze lange afstand te migreren. De zoetwaterfase van groei, geslachtsdifferentiatie en ‘schier’ worden, (een preadaptatie aan zijn oceanische fase en terugkeer naar zijn paaigronden) voor de migratie bepaalt uiteindelijk de kwaliteit van de ouderdieren. Deze periode in het zoete water kan een periode van 5-50 jaar beslaan. De kwaliteit van de ‘habitat’ (woonomgeving) en de kwaliteit van habitatfactoren zoals voedseltekort (wat leidt tot verminderde vetvoorraden), virussen en giftige stoffen (zoals PCB’s = polychloorbiphenyls) is belangrijk voor de zwemcapaciteit van de ouderdieren en de kwaliteit van de geslachtsproducten. In dit proefschrift zullen we de factoren die de levenscyclus van de Europese paling beschrijven, dit om meer begrip te krijgen voor de mogelijke factoren die betrokken zijn bij de afname van palingpopulaties en die betrokken zijn bij de reproductie. De zoetwaterfase, oriëntatie op het aardmagnetisch veld: In de literatuur zijn verschillende publicaties te vinden van veldstudies in bassins telemetrische studies, studies met sterke kunstmatige magnetische velden die de natuurlijke voorkeursrichting van paling overtreffen, die aangeven dat oriëntatie wordt bewerkstelligd door kenmerken van het aardmagnetisch veld. Ook de observatie van magnetische substanties in de schedel en botten van palingen ondersteunt in sterke mate deze zienswijze. Wij bestudeerden de circadiane (24-uurs) en maandelijkse activiteit, het distributiepatroon, en oriëntatie op het aardmagnetisch veld van niet-schiere (niet-migrerende) vrouwelijke paling op een zoetwatervijver door middel van microchips geïmplanteerd in hun spieren. Detectoren voor de microchips werden gemonteerd in buizen en deze worden op de vijver geplaatst om vast te stelen of palingen zich oriënteerden ten opzichte van het aardmagnetisch veld. Gebaseerd op de frequentie van het bezoeken van de buizen (corresponderend met het zoekgedrag naar een schuilplaats), gaven de data aan dat de aanwezigheid van de palingen in 1 Samenvatting de buizen geleidelijk afnam gedurende de duur van de studie. Daarnaast zagen we meer activiteit gedurende de nacht in de eerste paar maanden. Er was een seizoenscomponent in het oriëntatie mechanisme met een significant lagere voorkeurscomponent in de zomer in vergelijking tot de herfstperiode, de periode waarbij de migratie op gang komt. Een voorkeurspositie voor buizen georiënteerd in de Zuidzuidwestelijk richting (de richting van de Sargasso Zee) in de herfst suggereert een oriëntatie gebaseerd op het aard magnetisch veld. De zoetwaterfase: het schier worden De overgang van niet-schiere (niet-migrerende) naar schieraal (migrerend) wordt schier worden (‘silvering’) genoemd, en dit proces neemt plaats kort voor migratie. De mechanismen betrokken bij het in gang zetten van het schier worden zijn grotendeels onbekend. Ook een duidelijke beschrijving van de verschillende stadia, die de metamorfose karakteriseren ontbreken. Tot zeer recent werd het proces van schier worden voornamelijk gebaseerd op morfologische kenmerken en er werd een opsplitsing gemaakt in twee gescheiden stadia: ‘schier’ en ‘niet-schier’. Deze classificatie nam geen mogelijk voorbereidingsstadium in ogenschouw. Wij beschrijven hormonale profielen van Europese paling tijdens het proces van ‘schier’- worden. Wij hebben ook gebruik gemaakt in de beschrijving van fysiologische kenmerken als lichaamssamenstelling en bloedsubstraten. Deze transformatie gebeurd in associatie met hoge hormonale concentraties van testosteron (T), oestradiol (E2), cortisol maar niet met hoge concentraties van schildklierhormonen (TH) en groeihormoon (GH) welke een maximale activiteit hebben in het voorjaar en een minimale activiteit in de zomer en de herfst. In tegenstelling hiermee worden in de herfst hoge concentraties van cortisol gevonden welke een grote rol spelen in de mobilisatie van metabole energie van lichaamsvoorraden, naar migratie activiteit en de groei van de gonade. Gebaseerd op een statistische methode genaamd ‘Principal Component Analysis’
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